Spirulina enhanced the skeletal muscle protein in growing rats

Abstract

Background/Aim of the study

This study evaluates the effects of the blue green alga spirulina as the sole dietary source of protein on muscle protein in weaning rats.

Methods

Young (30 days) Wistar rats were fed, during 60 days, with 17% protein spirulina (S) and compared to rats fed 17% protein casein (C). We evaluated the muscle total protein and DNA contents and the in vitro protein synthesis and degradation rates as well the myosin protein expression.

Results

The groups presented similar body weight (C = 427.3 ± 8.6; S = 434.6 ± 7.7 g) and length (C = 25.4 ± 0.2; S = 25.6 ± 0.2 cm). Soleus muscle total protein (C = 2.9 ± 0.1; S = 2.7 ± 0.1 mg/100 mg) and DNA (C = 0.084 ± 0.005; S = 0.074 ± 0.005 mg/100 mg) contents were also similar in both groups. Protein degradation (C = 427.5 ± 40.6; S = 476.7 ± 50.5 pmol/mg−1 h−1) did not differ between the groups but protein synthesis (C = 17.5 ± 1.0; S = 25.2 ± 1.9 pmol/mg−1 h−1) and myosin content (western blot analyses) were higher (P < 0.05, t test) in spirulina group.

Conclusions

Although the spirulina proved adequate protein quality to maintain body growth, the muscle protein synthesis rates were increased by the ingestion of the experimental diet in young rats.

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References

  1. 1.

    Albanese AA, Orto, LA (1963) Protein and amino acids. In: Albanese AA (ed) Newer methods of nutritional biochemistry. Academic Press, New York, vol I. cap. 1, 84

  2. 2.

    Arvill A, Adolfsson S, Ahre′n K (1975) The use of the levator ani muscle in vitro in evaluating hormone action. Methods Enzymol 39:94–101

    Article  CAS  Google Scholar 

  3. 3.

    Bourges H, Sotomayor A, Mendonza E, Chavez A (1971) Utilization of the spirulina as a protein source. Nut Rep Int 4(1):31–42

    Google Scholar 

  4. 4.

    Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 7(72):48–54

    Google Scholar 

  5. 5.

    Branger B, Cadudal JL, Delobel M, Ouoba H, Yameogo P, Ouedraogo D (2003) Spiruline as a food supplement in case of infant malnutrition in Burkina-Faso. Arch Pediatr 10(5):424–431

    Article  CAS  Google Scholar 

  6. 6.

    Chen H, Pan SS (2005) Bioremediation potential of spirulina: toxicity and biosorption studies of lead. J Zhejiang Univ Sci B 6(3):171–174

    Article  CAS  Google Scholar 

  7. 7.

    Contreras A, Herbert DC, Grubs BG, Cameron IL (1979) Blue alga spirulina as the sole dietary source of protein in sexually maturing rats. Nut Rep Int 19(6):749–763

    CAS  Google Scholar 

  8. 8.

    Costa DA, De Morais MG, Dalcaton F, Reichert C, Durante AJ (2006) Simultaneous cultivation of spirulina plantesis and the toxigenic cyanobacteria microcystis aeruginosa. Z Naturforsch 61(1–2):105–110

    CAS  Google Scholar 

  9. 9.

    Coux O, Tanaka K, Goldberg AL (1996) Structure and functions of the 20S and 26S proteasomes. Ann Rev Biochem 65:801–847

    Article  CAS  Google Scholar 

  10. 10.

    Danzi S, Klein I (2005) Posttranscriptional regulation of myosin heavy chain expression in the heart by triiodothyromine. Am J Physiol Heart Circ Physiol 288(2):H455–H460

    Article  CAS  Google Scholar 

  11. 11.

    Dardevet D, Somet C, Balage M, Grizard J (2000) Stimulation of in vitro rat muscle protein synthesis by leucine decreases with age. J Nutr 130:2630–2635

    CAS  Google Scholar 

  12. 12.

    Deminge C, Block F, Picard N, Sabboh H, Besson C, Remesy C (2007) Mice chronically fed a westernized experimental diet as a model of obesity, metabolic syndrome and osteoporosis. Eur J Nutr 45(5):298–306

    Google Scholar 

  13. 13.

    Desai M, Crowter NJ, Lucas A, Hales CN (1996) Organ selective growth in the offspring of protein restricted mothers. Br J Nutr 76:591–603

    Article  CAS  Google Scholar 

  14. 14.

    Frayn KN, Maycock PF (1979) Regulation of protein metabolism by a physiological concentration of insulin in mouse soleus and extensor digitorium longus muscle. Biochem J 184:323–330

    CAS  Google Scholar 

  15. 15.

    Fulks RM, Li JB, Goldberg JL (1975) Effects of insulin, glucose, amino acids on protein turnover in rat diaphragm. J Biol Chem 250:290–298

    CAS  Google Scholar 

  16. 16.

    Furst PT (1978) Spirulina-nutritious alga, once a staple of Aztec diets could feed many of the world’s hungry people. Hum Nat 3:60–71

    Google Scholar 

  17. 17.

    Garlick PJ, Grant I (1988) Amino acid infusion increases the sensivity of protein synthesis to insulin. Effects of branched chain amino acids. Biochem J 254:579–584

    CAS  Google Scholar 

  18. 18.

    Giles A, Meyers A (1961) An improved diphenylamine method for the estimation of deoxyribonucleic acid. Nature 206(1 n. 4975):93

    Google Scholar 

  19. 19.

    Hadenshog G, Hofsten A (1979) The ultra structure of spirulina plantensis. A new source of microbial protein. Physiol Plant 23:209–216

    Article  Google Scholar 

  20. 20.

    Jeejeebhoy KN (2000) Nutritional assessment. Nutrition 16(7/8):585–590

    Article  CAS  Google Scholar 

  21. 21.

    Kapoor R, Metha U (1998) Supplementary effect of spirulina on hematological status of rats during pregnancy and lactation. Plant Foods Hum Nutr Aliment 29(6):517–534

    Google Scholar 

  22. 22.

    Kay RA (1991) Micro algae as food and supplement. Crit Rev Food Sci Nutr 30(6):555–573

    CAS  Article  Google Scholar 

  23. 23.

    Lang CH (2006) Elevated plasma free fatty acids decrease basal protein synthesis, but not the anabolic effect of leucine, in skeletal muscle. Am J Physiol Endocrinol Metab 291(3):E666–E674

    Article  CAS  Google Scholar 

  24. 24.

    Larbaud D, Debras E, Taillandier D, Samuels SE, Temparis S, Champredon C, Grizard J, Attaix D (1996) Euglycemic hyperinsulinemia and hyperaminoacidemia decrease skeletal muscle ubiquitin mRNA in goats. Am J Physiol 271:E505–E512

    CAS  Google Scholar 

  25. 25.

    Latorraca MQ, Reis MB, Carneiro EM, Mello MAR, Velloso LA, Saad MJ, Boschero AC (1998) Protein deficiency and nutritional recovery modulate insulin secretion and early steps of insulin action in rats. J Nutr 128:1643–1649

    CAS  Google Scholar 

  26. 26.

    Li ZY, Guo SY, Li L, Cai MY (2006) Effects of electromagnetic field on the batch cultivation and nutritional composition of spirulina plantesis in an air-lift photobioreactor. Bioresour Technol 98(3):700–705

    Article  CAS  Google Scholar 

  27. 27.

    Lowry OH, Rosebroug NJ, Farr AL, Randall RT (1951) Protein measurement with the folinphenol reagent. J Biol Chem 193:265–275

    CAS  Google Scholar 

  28. 28.

    Maranesi M, Barzanti V, Carenini G, Gentile P (1984) Nutritional studies on spirulina maxima. Acta Vitaminol Enzymol 6(4):295–304

    CAS  Google Scholar 

  29. 29.

    Martins MJ, Negrao MR, Hipolito-Reis C (2001) Alkaline phosphatase from rat liver and kidney is differentially modulated. Clin Biochem 34:463–468

    Article  CAS  Google Scholar 

  30. 30.

    Mello MAR, Luciano E, Carneiro EM, Latorraca MQ, Oliveira CAM, Boschero AC (2003) Glucose homeostasis in pregnant rats submitted to dietary protein restriction. Res Commun Mol Pathol Pharmacol 113–114:229–246

    Google Scholar 

  31. 31.

    Narayan MS, Manoj GP, Vatchravelo K, Bhagralakshmi N, Mahadevaswamy M (2005) Utilization of glycerol as carbon source on the growth, pigment and lipid production in spirulina plantesis. Int J Food Sci Nutr 56(7):521–528

    Article  CAS  Google Scholar 

  32. 32.

    Nogueira DM, Strufaldi B, Hirata M, Abdalla DS, Hirata RD (eds) (1990) Métodos de Bioquímica Clínica, São Paulo, Pancas Editorial

  33. 33.

    Prada FJ, Luciano E, Carneiro EM, Boschero AC, Mello MAR (2001) Protein deficiency attenuates the effects of alloxan on insulin secretion on glucose homeostasis in rats. Physiol Chem Phys Med NMR 33:73–82

    CAS  Google Scholar 

  34. 34.

    Proud CG (2006) Regulation of protein synthesis by insulin. Biochem Soc Trans 34(2):213–216

    Article  CAS  Google Scholar 

  35. 35.

    Reeves PG, Nielsen FH, Fahey GC (1993) AIN-93 purified diets for laboratory rodents: final reports of the American Institute of Nutrition ad hoc Writing Committee on the reformulation of the AIN-76 rodent diet. J Nutr 123:1939–1951

    CAS  Google Scholar 

  36. 36.

    Salazar M, Chamorro GA, Salazar S, Steele CE (1996) Effects of spirulina maxima consumption on reproduction and peri and post natal development in rats. Food Chem Toxicol 34(4):353–359

    Article  CAS  Google Scholar 

  37. 37.

    Sautier C, Tremolieres J (1975) Food value of the spirulina algae to man. Ann Nutr Aliment 29(6):517–534

    CAS  Google Scholar 

  38. 38.

    Seider MJ, Kapp R, Cheg CP, Booth FW (1980) The effect of cutting or stretching skeletal muscle in vitro on the rates of protein synthesis and degradation. Biochem J 188:247–254

    CAS  Google Scholar 

  39. 39.

    Silva RG, Almeida CCA, Luciano E, Mello MAR (2000) Protein malnutrition does not impair glucose metabolism adaptations to exercise training. Nutr Res 20(4):527–535

    Article  Google Scholar 

  40. 40.

    Simpore J, Zongo F, Kabore F, Dansou D, Bere A, Nikiema JB, Pignatelli S, Biondi DM, Ruberto G, Musumecis S (2005) Nutrition rehabilitation of HIV-infected and HIV-negative undernourished children utilizing spirulina. Ann Nutr Metab 49(6):373–380

    Article  CAS  Google Scholar 

  41. 41.

    Simpore J, Kabore F, Zongo F, Dansou D, Bere A (2006) Nutrition rehabilitation of undernourished children utilizing spirulina and misola. Nutr J 23(5):3–9

    Article  CAS  Google Scholar 

  42. 42.

    Stevanato E, Gobatto CA, Mello MAR, Kokubun E (1998) Free fatty acid concentration did not affect carbohydrate metabolism in soleus muscle in vitro. Med Sci Sport Exerc 30:S247

    Article  Google Scholar 

  43. 43.

    Svanberg E, Svaninger G, Soussi B, Lundholm K (1999) Mouse extensor digitorium muscle preparation as a tool in nutrition research: a quantitative comparison to in vivo and cell culture experiments. Nutrition 15:200–207

    Article  CAS  Google Scholar 

  44. 44.

    Torun B, Chew F (1994) Protein energy malnutrition. Mod Nutr Health Dis 2:950–976

    Google Scholar 

  45. 45.

    Tranquille N, Emeis JJ, Chambure D, Binot R, Tamponnet C (1994) Spirulina acceptability trials in rats. A study for the “Melissa” life-support system. Adv Space Res 14(11):167–170

    Article  CAS  Google Scholar 

  46. 46.

    Waalkes TP, Udenfriend S (1957) Tyrosine in plasma and tissues. J Lab Clin Med 50(5):733–736

    CAS  Google Scholar 

  47. 47.

    Winick M, Basel JA, Rosso P (1972) A nutrition and cell growth. In: Winick M (ed) Nutrition and development. Wiley, New York, pp 49–97

    Google Scholar 

Download references

Acknowledgments

The authors want to thank the Brazilian Foundation Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for financial support.

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Correspondence to Fabrício A. Voltarelli.

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Voltarelli, F.A., de Mello, M.A.R. Spirulina enhanced the skeletal muscle protein in growing rats. Eur J Nutr 47, 393–400 (2008). https://doi.org/10.1007/s00394-008-0740-9

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Keywords

  • skeletal muscle
  • spirulina
  • protein